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Camouflage in Predators CORE Metadata, citation and similar papers at core.ac.uk Provided by St Andrews Research Repository Biol. Rev. (2020), pp. 000–000. 1 doi: 10.1111/brv.12612 Camouflage in predators Matilda Q. R. Pembury Smith* and Graeme D. Ruxton School of Biology, University of St Andrews, Dyers Brae House, St Andrews, Fife, KY16 9TH, U.K. ABSTRACT Camouflage – adaptations that prevent detection and/or recognition – is a key example of evolution by natural selection, making it a primary focus in evolutionary ecology and animal behaviour. Most work has focused on camouflage as an anti-predator adaptation. However, predators also display specific colours, patterns and behaviours that reduce visual detection or recognition to facilitate predation. To date, very little attention has been given to predatory camouflage strategies. Although many of the same principles of camouflage studied in prey translate to predators, differences between the two groups (in motility, relative size, and control over the time and place of predation attempts) may alter selection pressures for certain visual and behavioural traits. This makes many predatory camouflage techniques unique and rarely documented. Recently, new technologies have emerged that provide a greater opportunity to carry out research on natural predator–prey interactions. Here we review work on the camouflage strategies used by pursuit and ambush predators to evade detection and recognition by prey, as well as looking at how work on prey camouflage can be applied to predators in order to understand how and why specific predatory camouflage strategies may have evolved. We highlight that a shift is needed in camouflage research focus, as this field has comparatively neglected cam- ouflage in predators, and offer suggestions for future work that would help to improve our understanding of camouflage. Key words: camouflage, crypsis, predation, behaviour, movement, mimicry, evolution CONTENTS I. Introduction .........................................................................2 II. Ambush predators .....................................................................2 (1) Aggressive crypsis ................................................................. 3 (2) Aggressive masquerade ............................................................. 4 (3) Aggressive mimicry ................................................................ 4 (a) Aggressive mimicry without a lure .................................................. 4 (b) Aggressive mimicry using a generalised lure .......................................... 5 (c) Aggressive mimicry using a specialised lure ........................................... 5 III. Pursuit predators ......................................................................6 (1) Dynamic crypsis via background-matching .............................................. 6 (2) Dynamic crypsis via disruptive colouration .............................................. 6 (3) Motion masquerade ................................................................ 7 (4) Motion camouflage ................................................................ 8 IV. Factors affecting the evolution of camouflage strategies in predators ..............................9 (1) Time of attack .................................................................... 9 (2) Size ........................................................................... 10 (3) Prey ........................................................................... 10 (4) Environment .................................................................... 12 V. Conclusions .........................................................................12 VI. References ..........................................................................13 * Address for correspondence (Tel: +44 (0) 7503152203; E-mail: [email protected]) Biological Reviews (2020) 000–000 © 2020 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 2 Matilda Q. R. Pembury Smith and Graeme D. Ruxton I. INTRODUCTION arise are key examples of evolution by natural selection (Wallace, 1889; Poulton, 1890; Cott, 1940), camouflage as an Animal camouflage is a morphological adaptation which anti-predator strategy is heavily documented in the literature. describes all forms of concealment that hinder detection Many predators also display specific colours, patterns and and recognition (Merilaita & Stevens, 2011). Predation, a behaviours that appear to reduce visual detection or recognition biological interaction in which one organism kills another to improve prey-capture success. Although some predator sys- for food, is likely to be one of the strongest selective forces tems have been analysed, less attention has been given overall in nature. Camouflage is often considered a critical compo- to predatory camouflage strategies, likely a result of increased nent of both prey and predator survival strategies challenges when monitoring predatory behaviour. The terri- (Cott, 1940; Endler, 1981; Stevens & Merilaita, 2009; Rux- tories of large predators span wide geographical areas, making ton, Sherratt & Speed, 2004). observations of natural predation events difficult, and their large Although camouflage is used as an umbrella term to describe size means handling can impose a risk to the investigator. Most all strategies that prevent detection and recognition, there are predation events are hard to predict, as some predatory strate- many different ways in which organisms can conceal them- gies are only expressed at the onset of an attack. It can also be selves. The most commonly documented is crypsis: adaptations difficult to identify whether a particular trait has evolved to involving body colouration that delay detection (Endler, 1978; reduce detection by prey or detection by another predator, as Merilaita & Stevens, 2011; Merilaita, Scott-Samuel & non-apex predators will operate under both selection pressures. Cuthill, 2017; Ruxton et al., 2004). There are many forms of Despite these challenges, camouflage in predators is important crypsis, the best known being background-matching whereby to document. Although many of the same principles studied in an organism matches the colour and pattern of their surround- prey, such as minimising detection and or recognition, also ings (Stuart-Fox, Moussalli & Whiting, 2008; Merilaita & apply to predators, the purpose of camouflage in predators is Stevens, 2011; Ruxton & Stevens, 2015; Kang, Kim & to gain close proximity to prey. Pursuit and ambush predation Jang, 2016). Others include: disruptive colouration, where use different strategies to achieve this goal, giving rise to a vari- an organism displays a highly contrasting colour pattern in ety of unique adaptations. Predators are also generally larger order to break up their body outline (Cuthill et al., 2005; than their prey. Although research on the role of size on camou- Schaefer & Stobbe, 2006; Stevens & Cuthill, 2006); self- flage is limited, it has been established that larger organisms are shadow concealment (Wilkinson & Sherratt, 2008; Kelley & more conspicuous in comparison to small organisms Merilaita, 2015; Caro, 2016), in which colour patterns (nor- (Main, 1987), meaning that predators must evolve ways in mally a dark upper surface colour and a pale underside) which to remain camouflaged despite their size. Finally, as pred- reduce detection by subverting variation in shadowing that is ators are at liberty to choose when and where to attack their used to separate objects visually from their background prey, they only need to avoid detection during these specific (Chapman, Kaufman & Chapman, 1994; Stauffer, Hale & times and locations. By contrast, prey species need to maintain Seltzer, 1999); transparency (Mackie & Mackie, 1967; camouflagemoreconsistentlyastheyhavealimitedabilityto Johnsen, 2001); silvering/mirrors (Denton, 1970, 1971) and predict the presence of a threat. This enables predators to self-decoration (Allgaier, 2007; Yanes et al., 2009). fine-tune their camouflage strategy to specific situations, unlike Despite camouflage research predominantly focusing on prey which have to achieve successful camouflage over a range the efficacy of crypsis strategies, there are many other forms of contexts. These differences between predators and prey may of camouflage that do not prevent initial detection. They alter the selection pressures for certain visual and behavioural instead interfere with an organism’s cognitive processes traits, making many predatory camouflage strategies unique. rather than sensory processes, in order to reduce recognition This review analyses anti-detection and anti-recognition or capture success. Examples include masquerade, in which strategies in ambush and pursuit predators, focusing on the the organism resembles another object (Endler, 1981; Allen & differences and similarities between the selection pressures Cooper, 1985; Edmunds, 1990; Skelhorn et al., 2010), dazzle they face, and how these contrast with those experienced by camouflage, in which detection occurs but colour patterns or prey. The diversity of camouflage strategies in predators movement confuse the detector as to the animal’s speed and highlights the importance of minimising detection by prey. direction (Thayer, 1909; Jackson, Ingram & Campbell, 1976; As some predatory
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